Heat-avoidance behavior associates with thermal sensitivity rather than tolerance in aphid assemblages

How to predict animals’ heat-avoidance behaviors is critical since behavior stands the first line for animals dealing with frequent heat events under ongoing climate warming. However, the discrepancy between the scarcity of research on heat-avoidance behaviors and the commonness of eco-physiological data for thermal tolerance and for thermal sensitivity such as the temperature-dependent survival time makes it difficult to link physiologically thermal traits to heat-avoidance behavior. Aphids usually suck plant sap on a fixed site on the host plants at moderate temperatures, but they will leave and seek cooler feeding sites under stressful temperatures. Here we take the cereal aphid assemblages comprising different species with various development stages as a model system. We tested the hypotheses that heat tolerance (critical thermal maximum, CTmax) or heat sensitivity (temperature-dependent declining rate of survival time, similarly hereinafter) would associate with the temperature at which aphid activate heat-avoidance behavior. Specifically, we hypothesized the aphids with less heat tolerance or greater heat sensitivity would take a lower heat risk by leaving the host plant earlier. By mimicking the linear increase in ambient temperature during the daytime, we measured the CTmax and the heat-avoidance temperature (HAT, at which aphids leave the host plant to find cooler places) to understand their heat tolerance and heat-avoidance behavior. Then, we tested the survival time of aphids at different temperatures and calculated the slope of survival time declining with temperature to assess their heat sensitivity (HS). Finally, we examined the relationships between CTmax and HAT and between HS and HAT to understand if the heat-avoidance behavior associates with heat tolerance or with heat sensitivity. The results showed that HS and HAT had a strong correlation, with more heat sensitive individuals displayed lower HAT. By contrast, CTmax and HAT had a weak correlation. Our results thus provide evidence that heat sensitivity is a more reliable indicator than thermal tolerance linking with the heat-avoidance behavior in the aphid assemblages. Most existing studies use the indexes related to thermal tolerance to predict warming impacts. Our findings highlight the urgency to incorporate thermal sensitivity when predicting animal responses to climate change.

如何预测动物的热回避行为（heat-avoidance behaviors）至关重要，因为在当前气候变暖背景下，行为是动物应对频繁热事件的第一道防线。然而，热回避行为研究的稀缺性与热耐受性（thermal tolerance）、热敏感性（thermal sensitivity）等生态生理数据（如温度依赖性存活时间，temperature-dependent survival time）的普遍性之间存在差异，这使得将生理热性状与热回避行为关联起来面临挑战。蚜虫在适宜温度下通常固定于寄主植物某一位点吸食汁液，但在胁迫温度下会离开并寻找更凉爽的取食位点。本研究以包含不同物种及发育阶段的麦蚜集合体为模型系统，验证以下假设：热耐受性（以临界热最大值，critical thermal maximum，CTmax表示）或热敏感性（以存活时间随温度下降的速率表示，下文同）与蚜虫启动热回避行为的温度相关。具体而言，我们推测热耐受性较弱或热敏感性较强的蚜虫会通过更早离开寄主植物降低热风险。通过模拟日间环境温度的线性升高，我们测定了CTmax与热回避温度（heat-avoidance temperature，HAT，即蚜虫离开寄主植物寻找凉爽场所的温度），以解析其热耐受性与热回避行为特征；随后测定蚜虫在不同温度下的存活时间，计算存活时间随温度下降的斜率以评估热敏感性（HS）；最终分析CTmax与HAT、HS与HAT的关系，明确热回避行为与热耐受性或热敏感性的关联。结果显示，HS与HAT呈强相关，热敏感性越强的个体HAT越低；而CTmax与HAT的相关性较弱。因此，本研究证明在麦蚜集合体中，热敏感性是比热耐受性更可靠的热回避行为关联指标。现有多数研究采用热耐受性相关指标预测变暖影响，而我们的发现强调了在预测动物对气候变化响应时纳入热敏感性的迫切性。